Educating undergraduate medical students about oncology. a literature review, jco 2006

Educating Undergraduate Medical Students About
Oncology: A Literature Review
Judith Gaffan, Jane Dacre, and Alison Jones
A B S T R A C T
Purpose
This article is a review of the literature regarding teaching oncology to undergraduate medical students.
Methods
MEDLINE, Psychinfo, ERIC, TIMELIT, EMBASE, CINAHL and the Cochrane CENTRAL Register of
Controlled Trials (CENTRAL) were searched, using the search terms cancer, oncology, education,
undergraduate, and teaching.
Results
The main findings can be summarized as follows: the involvement of patients in teaching is
popular with students and portfolio learning is a successful way of involving patients; the use of
standardized patients to teach breast examination improves students’ performance in clinical
assessment; the use of silicone models to teach breast examination improves students’ sensitivity
for detecting breast lumps; computer aided learning modules have a role, but are not superior to
other types of learning; learning about cancer screening and prevention increases students’
knowledge, improves their self rated skills, and changes their behavior; and cancer patients have
an important role to play in teaching undergraduate communication skills.
Conclusion
We have found 48 articles on undergraduate teaching in oncology. Oncology teachers should
consider adopting the evidence based approaches outlined in this review, and there should be
more emphasis on educational research within the field of oncology.
J Clin Oncol 24:1932-1939. © 2006 by American Society of Clinical Oncology
INTRODUCTION
This is a review of the teaching oncology to under-
graduate medical students literature. It is important
that all medical students learn about cancer as all
qualified doctors encounter patients with cancer,
but only those with an interest in oncology receive
specialized postgraduate training.
Most oncologists are involved in providing
undergraduate level education. A 1993 survey
of oncology departments found that 78% of med-
ical oncology and 53% of clinical oncology
departments had regular commitments to teach-
ing.1
The time devoted by oncologists to teach-
ing is likely to have increased since the survey
was performed because the number of students
at medical school has increased by 55% since
1997.2
However, there is no consensus on what
should be learned at the undergraduate level, or
what the best and most appropriate teaching
methods are.
Theaimofthisreviewistofacilitateundergrad-
uate education in oncology by informing curricu-
lum design, stimulating ideas for innovations in
teaching, and making the literature on oncology ed-
ucation more accessible.
Background
Medical education has changed from being a
teacher-centered process to a learner-centered pro-
cess(focusingonwhatthestudentslearnratherthan
what the educator teaches). Lectures are being
phased out in favor of small group work and experi-
ential learning. Medical training is now recognized
as a life-long process, encouraging students to be-
come reflective practitioners. There is increasing
emphasisonteachingandassessingvalues,attitudes,
and beliefs.3,4
Oncology is a multidisciplinary specialty,
which occurs throughout the curriculum. Hence,
teaching may be fragmented, with an overlap in
the fields of surgery, pathology, communication
skills, and palliative care. A high proportion of
patients with cancer are being managed as outpa-
tients, making it harder for medical students to
observe them.
From the Academic Centre for Medical
Education, Royal Free and University
College Medical School Archway
Campus; and the Royal Free and
University College London Medical
School, London, United Kingdom.
Submitted May 11, 2005; accepted
February 15, 2006.
Supported by a fellowship from Cancer
Research United Kingdom.
Authors’ disclosures of potential con-
flicts of interest and author contribu-
tions are found at the end of this
article.
Address reprint requests to Judith
Gaffan, ACME, Royal Free & University
College Medical School, Archway
Campus, 4th Floor Holborn Union Build-
ing, Highgate Hill, London N19 5LW,
United Kingdom; e-mail: j.gaffan@
medsch.ucl.ac.uk.
© 2006 by American Society of Clinical
Oncology
0732-183X/06/2412-1932/$20.00
DOI: 10.1200/JCO.2005.02.6617
JOURNAL OF CLINICAL ONCOLOGY R E V I E W A R T I C L E
VOLUME 24 ⅐ NUMBER 12 ⅐ APRIL 20 2006
1932
Downloaded from ascopubs.org by Marcela Kober on February 16, 2018 from 190.193.234.068
Copyright © 2018 American Society of Clinical Oncology. All rights reserved.

Search Strategy and Selection Criteria
Studies were identified by searching MEDLINE, Psychinfo,
ERIC, TIMELIT, EMBASE, CINAHL, the Cochrane CENTRAL
Register of Controlled Trials (CENTRAL), and reference lists from
relevant articles, using the search terms shown in the data supple-
ment. For ERIC and TIMELIT, it was not necessary to include the
catch all educational search terms because they are databases of
educational literature.
Published abstracts without complete articles were excluded be-
cause of the inability to obtain detailed information regarding partic-
ipants and interventions. The search was restricted to articles dated
from January 1, 1993, to August 1, 2004. The abstracts of the articles
identifiedwerereadandarticleswereselectedaccordingtothefollow-
ing criteria.
Inclusion Criteria
Inclusion criteria included: studies evaluating oncology teach-
ing interventions; descriptive studies (interventions with before
and after, or after alone evaluations), cohort studies, and interven-
tion/control or randomized controlled trials; studies where all (or a
significant and identifiable proportion) of the participants were
medical students; and studies where the participants were doctors
in their first year of practice.
Exclusion Criteria
Exclusion criteria included: studies where the participants were
senior house officers, residents, senior doctors, dentistry or nursing
students, or patients; multiple publications referring to the same in-
tervention (only the most comprehensive or conclusive studies were
included); studies of interventions to teach palliative or supportive
care (this topic has been reviewed elsewhere);5
and studies where the
intervention was not evaluated.
Justification for the Restriction on Publication Date
In 1993, the General Medical Council published a comprehen-
sive review of medical education.6
All medical schools in the United
Kingdom have changed their undergraduate teaching significantly in
response.2
Therefore,thisreviewisrestrictedtostudiespublishedafter
the General Medical Council guidance was issued.
RESULTS
The search resulted in 81 abstracts, 33 of which were excluded after
readingthefull-textarticles.Thereasonsforexclusionarepresentedin
the data supplement, but the most common reason (20 articles) was
that the participants were not medical students.
Thosearticlesthatarerevieweddividednaturallyintofivesubject
areas:oncologycourses/attachments/electives;teachingaboutspecific
types of cancer; cancer screening and prevention; examination skills
necessary for cancer detection; and communication skills.
Oncology Courses, Attachments, and Electives
Thirteen articles that describe oncology courses were found. The
courses range from portfolio learning to summer schools, and these
articles are summarized in Table 1.
Table 1. Oncology Courses, Attachments, and Electives
Study Design
No. of
Students Intervention Outcome Measure Outcome
De Vries18
DES 39 Oncology summer school Knowledge test before and after and
student satisfaction
Improvement in knowledge (P ϭ .001)
Barrett17
DES NS Oncology attachment Student satisfaction Rated as the best part of their curriculum
(1998)
Smith20
DES 24 Oncology attachment Knowledge tests before, after and at
6 months
Knowledge rose by 40% (P Ͻ .01); 90%
of knowledge retained at 6 mo
Jazieh19
DES 16 Oncology summer elective Knowledge tests before and after Scores rose from 46.6% before to 53%
afterwards (P ϭ .001)
Plymale10
DES 124 Oncology module taught by
cancer patients
Satisfaction of students and cancer
patients
Students gave module 4.4/5 (Likert scale)
Mota11
DES 12 Student-staffed oncology clinic Student and patient satisfaction 92% of students felt it was the best part
of their curriculum
Mehta14
Int/Con 164 Intervention group: 35 h Web-
based learning tool; control
group: normal teaching
Knowledge test before and after and
Knowledge equivalent in the two groups
and feedback positive
Finlay7
RCT 159 Intervention group: each
student followed a patient
with cancer for 9 mo; control
group: normal teaching
Hidden questions in final year OSCE Overall trend to improved scores for
intervention group (most marked for
lowest achievers)
Blair13
DES 275 Use of computer information
system
Student satisfaction 87% of students said course was valuable
Besa12
DES NS CAL module on oncology Student satisfaction Students gave course 4.1/5 for design and
3.88/5 for applicability (Likert scale)
Conatser9
Des 23 Students followed up children
with cancer
Student and parent satisfaction Positive feedback
Axelrod16
DES 49 Summer oncology fellowship Student satisfaction Positive feedback
Fukuchi15
DES 16 Interactive computer assisted
board game
Before and after performance at
game, student feedback
Performance improved; students reported
increased awareness of
multidisciplinary nature of oncology
Abbreviations: DES, descriptive; NS, not stated; Int/Con, intervention and control arm; h, hour; RCT, randomized controlled trial; mo, month; OSCE, objective
structured clinical examination; CAL, computer aided learning.
Teaching Medical Students About Oncology
www.jco.org 1933

Portfolio learning. A portfolio is a collection of material made by
a student over a period of time, and is based on their experiences.
There are two trials of portfolio learning in oncology.
Finlay et al randomly assigned 159 medical students to inter-
vention (portfolio) or control (standard) oncology teaching.7
The
portfolio group was assigned a patient with cancer to follow for 9
months. The students attended their patient’s clinic visits, scans,
and home visits (if appropriate), and produced a portfolio of
written work consisting of reflections on their interactions with the
patient, commentary on the cancer, press cuttings, and photo-
graphs. The control group received the standard oncology curric-
ulum. The portfolio learning was popular—90% of students felt
that it was a worthwhile and valuable experience.8
In the assess-
ment, there was a trend for the intervention group to perform
better in oncology questions.
In a cohort study of portfolio learning in Texas, 23 medical
students were paired with children who had cancer or other chronic
illnesses.9
The evaluation of this project was qualitative, and the feed-
back was positive. The main advantage of pairing students and chil-
dren was that real friendships, often based on fun, could develop.
The standardized use of cancer patients in teaching. Most clinical
teaching involves patients in an opportunistic way. Two groups of
researchers have designed oncology teaching interventions, which
involve patients in a more standardized way. In South Carolina, 42
trainedcancersurvivorstaughtstructuredcancerskillscoursesfor124
medical students.10
Plymale et al’s primary outcome measure was the
satisfactionofthecancersurvivors,andthiswashigh:63%ofsurvivors
described the experience as outstanding, and 100% of survivors said
they would be willing to help again.
A Brazilian medical school piloted a student-staffed oncology
clinic.11
In this clinic, 12 medical students assessed the patients,
planned the treatment, and prescribed the chemotherapy. They were
closely supervised. Ninety-three cycles of chemotherapy were pre-
scribed to 53 patients, without any adverse incidents. Ninety-two
percent of students rated the teaching clinic the best thing they had
done in medical school.
Computer aided learning. Four articles describe computer aided
learning modules for teaching oncology.12-15
None of the authors
were able to demonstrate that computer aided learning resulted in
better knowledge retention than more traditional forms of teach-
ing, but all reported that student feedback was positive. Besa et al12
developed a cancer learning center similar to a clinical skills center,
involving several computer aided learning tutorials. Some tutorials
involved manikins; for example, a sigmoidoscope and a model
colon with lesions. In the feedback, the students were particularly
enthusiastic about the tutorials with manikins.
Summer schools and electives. Five articles describe short courses
inoncology.16-20
Theaimsofthesecoursesinclude:teachingoncology
skills for primary care18-20
; encouraging students to take up careers in
oncology16
; and encouraging an interest in research.19
Student feed-
back was positive after all of the courses, and when knowledge was
tested, it was increased.18-20
The courses used a wide range of educa-
tionalactivitiesincludingclinics,multidisciplinarymeetings,problem
based learning, journal clubs, projects, and poster presentations. It is
notpossiblefromreadingthearticlestoascertainwhichactivitieswere
most valuable.
Teaching About Specific Types of Cancer
Eight articles describing different interventions to teach about
specific cancers including breast, prostate, and ovarian cancer were
found (Table 2 for summary).
Drama. A 1-hour theater performance was given by an ovarian
cancer survivor to a mixed audience including faculty and students.21
The performance was followed by a 30-minute panel discussion. The
feedback was positive and the attendees felt the performance would
influence their clinical practice (Likert scale mean, 4.7 of 5).
Structured clinical instruction modules. The structured clinical
instruction module (SCIM) is a teaching method developed in Ken-
tucky. Students rotate around several 10-minute teaching stations
performing tasks (eg, mammogram interpretation) and receiving
feedback. A breast cancer SCIM was first published as a pilot study
in 1997.22
The SCIM was then incorporated into a breast cancer
Table 2. Teaching About Specific Types of Cancer
Study Design
No. of
Seabra26
Int/Con 60 Intervention group: CAL module
about prostate cancer; control-
normal teaching
Knowledge test after
intervention and
Test performance similar in two groups
Shapiro21
DES 20 Theatrical performance about
ovarian cancer
Student satisfaction Positive feedback
Miedzybrodzka24
RCT 171 Intervention group: CAL module
about familial breast cancer;
control group: normal teaching
Knowledge test after
intervention and
No difference between the two groups
Plymale23
DES 30 4 part program including lecture,
SCIM, PBL, and manual
Student satisfaction Students expressed preference for the
SCIM over other teaching
Sloan22
DES 30 Breast cancer SCIM Student, patient, and
faculty satisfaction
Positive feedback
Teague59
DES 173 Small group discussion of
genetic cases
Knowledge tests
before and after
Scores increased from 58% before to
85% after (P Ͻ .01)
Mooney25
DES 51 Electronic study guide on breast
cancer
Student satisfaction Positive feedback
Sneiderman27
DES 165 CAL tutorial on malignant
melanoma
Student satisfaction Some negative technical comments
Abbreviations: Int/Con, intervention and control arm; CAL, computer aided learning; DES, descriptive; RCT, randomized controlled trial; SCIM, structured clinical
instruction module; PBL, problem-based learning.
Gaffan, Dacre, and Jones
1934 JOURNAL OF CLINICAL ONCOLOGY

educational package; it was the most popular part of the package,
scoring4.6of5onaLikertscale.23
Incomparison,lecturescored4.0of
5, and problem based learning scored 3.6 of 5.
Computer aided learning in specific cancers. Computer aided
learning courses on breast cancer, prostate cancer, melanoma, or
familial cancer are described.24-27
None of the authors were able to
show that computer aided learning improved student learning, in-
cluding the randomized trial with 171 students.24
However, in the
randomized trial attendance was only 27% and 28% in the two arms.
Teaching About Cancer Screening and Prevention
Four articles on teaching cancer screening and prevention were
found,andtheyaresummarizedinTable3.Teachingcancerscreening
and prevention can increase medical student’s knowledge28,29
and
self-rated skills30,31
and change their behavior.28
A 1-week course on
sun awareness increased students knowledge about sun protection,
and after the course the students reported fewer episodes of sun-
burn and significantly more use of sun protection. These changes
in the student’s behavior were sustained 1 year later.28
At Boston
University Medical School, after increasing the number of hours
on cancer prevention from 6 to 15, the percentage of students who
reported that they had already practiced cancer prevention rose
from 53% to 83% (P Ͻ .001).31
Learning Examination Skills Necessary for
Cancer Detection
Eleven articles on teaching examination techniques were found,
and they are summarized in Table 4.
The use of manikins. Silicone models, dynamic models, and a
home study module have been used to teach breast examination.32-35
The use of training models improved students ability to detect
lumps.32,34,35
However, the outcome measure was performance using
the models, and because only the intervention group had used the
model before, the control group was at a systematic disadvantage.
A testicular examination manikin named Zack, who has one
normal and one lumpy testicle, has also been evaluated.36
The student
feedback was positive.
The use of standardized patients. Four studies found that using
standardized patients to teach breast evaluation skills is acceptable
and feasible. Students who were taught by standardized patients
performed better in a clinical skills examination.37-40
Twostudiesrandomlyassignedstudentstoreceivetheirteaching
from standardized patients or from faculty, and then compared the
students’abilitytodetectlumpsinabreastmodel.Thestudentstaught
by the standardized patients detected more lumps.37,39
Learning about pigmented skin lesions. Cliff et al41
gave a lecture
andanillustratedbookletonpigmentedskinlesionsto27students(no
control group). The students’ diagnostic accuracy improved signifi-
cantly after the intervention (P ϭ .001).
Learning Communication Skills for Oncology
Twelve articles on teaching communication skills were found,
and they are summarized in Table 5. We also found four previous
reviews about communication skills teaching.42-45
The reference lists
of these reviews were searched, and relevant articles included.
Communicating with patients with cancer. Klein et al randomly
assigned students to communication skills teaching with either
patients with cancer patients or other patients, and then observed
them for 2 years.46
Students in the cancer group were more likely to
respond empathetically to patients, and more likely to express favor-
able attitudes (eg, listening to patients is important.)
Three other studies describe the successful use of role play to
teach oncology specific communication skills.47-49
Givingbadnews. Roleplaysofcancer-relatedscenarioshavealso
been used to teach students how to give bad news.50-55
In one study,
trained patients with cancer were used in the role plays.54
Colletti et al showed that the ability to give bad news was trans-
ferable from cancer scenarios to other scenarios.55
Their intervention
students (trained in giving bad news) performed significantly better
than their control students (untrained). The training scenarios
involved either cancer or a miscarriage, but all students were eval-
uated using the miscarriage scenario. Within the intervention
group, the cancer-trained students performed as well as the
miscarriage-trained students.
Summary of Results
Theinvolvementofpatientsinteachingandlearninginoncology
is popular with students, and where patient satisfaction has been
tested, it has also been found to be high. Several authors have investi-
gated methods of standardizing the involvement of patients (eg, by
training patients to take a specific role in the teaching or giving stu-
dents a particular learning objective to achieve with a particular
Table 3. Teaching About Cancer Screening and Prevention
Study Design
No. of
Madan29
DES 27 60 min structured lecture on
breast cancer screening
Pre- and postknowledge test;
Knowledge scores increased from 84% to
93% (P ϭ .0016); 96% of students said
the course should be offered routinely
Geller31
Cohort 600 Implementation of a cancer
prevention curriculum and
increasing the hours of
cancer prevention education
from 6 h to 15 h
Student’s perceived competence,
knowledge, and satisfaction
Students who had completed the altered
curriculum felt more confident, and
their perceived knowledge increased
Liu28
DES 98 1 wk sun awareness course Knowledge before, after and at 1 yr;
self-reported sun protection
behavior
Knowledge increased (62% pre, 89%
post, and 73% at 1 year P Ͻ .01);
sun-protection behavior increased
Geller30
DES 246 Cancer skills laboratory
consisting of 2 h of teaching
in 15 min stations
Before and after testing of self-rated
ability to perform clinical skills
Self-rated skill increased from 2.1/5 to
3.8/5 (P Ͻ .001)
Abbreviations: DES, descriptive; min, minute; cohort, trial comparing two cohorts of students; h, hour; wk, week; yr, year.
www.jco.org 1935

patient). There is a trend toward improved performance in assess-
ments after portfolio learning based around the follow-up of a single
patient with cancer.
Studentslearningbreastexaminationfromstandardizedpatients
performbetterthanstudentstaughtbyfaculty(asassessedbyaclinical
examination). Students learning breast examination by using silicone
models have higher sensitivity for detecting breast lumps (as assessed
by ability to detect lumps in silicone breast models). Computer-aided
learning modules have a role, but are not superior to other types of
learning; learning about cancer screening and prevention increases
students’ knowledge, improves their self rated skills, and changes
their behavior. Students who learn communication skills from
patients with cancer have better skills and attitudes than students
learning from noncancer patients.
DISCUSSION
Despite the fact that most oncology departments are involved in
teaching1
only 48 studies of interventions for teaching oncology to
medical students have been found. It is possible that we may have
missed some relevant studies by using a free text search rather than
index terms, or by not searching for some words, phrases, and index
terms that would be specific to education about particular cancer
related topics (eg, mammography). However, it is likely that there is
extensive good teaching practice in use, which is not documented or
published, so it is important to discuss potential barriers to the publi-
cation of research into teaching oncology. Teaching innovations tend
to be implemented in a nonsystematic way, making the outcomes
difficult to publish. Oncologists are not routinely encouraged to learn
the methodology for educational research. Research into teaching is
undervalued in the oncology community. Many of the articles in this
review are published in journals that are low on the citation index
(median impact factor, 1.156
), which reduces their perceived worth.
Therearebarriersalsototheadoptionofevidencebasedteaching
methods in oncology. The quality of the trials presented here is vari-
able. Many of the studies are descriptive, so it is difficult to draw
conclusions about best teaching practices. Of studies presented here,
only 13 (27%) of 48 had control groups, and in only seven of 48 were
students randomly assigned to intervention or control. Student feed-
back is the only end point in 16 of 48 studies, and the feedback was
overwhelmingly reported as positive. Other authors have found sim-
ilarlimitations–areviewofcommunicationskillsteachingfound21%
Table 4. Teaching Examination Skills Necessary for Cancer Detection
Study Design
No. of
Taylor36
DES NS Testicular examination model Student satisfaction Positive feedback
Gerling34
Int/Con 48 Standard versus dynamic models to
teach breast examination
Ability to detect lumps in
breast models
Lump detection higher for group
trained with dynamic model
(P Ͻ .001)
Cliff41
DES 27 Lecture and illustrated booklet on skin
cancer
Pre- and postrecognition of
skin lesions
Increase in correct diagnoses
(P Ͻ .001)
Madan35
Int/Con 47 Intervention group: breast examination
video and teaching with a model;
Control group: no teaching
Pre- and post-testing of ability
to detect lumps in breast
models
Significant improvement in lump
detection for intervention
group (P Ͻ .05)
Aliabadi-Wahle32
RCT 30 Intervention group: 1 h teaching on
breast examination; control group:
no teaching
breast models
detection in intervention
group (P Ͻ .01)
Harris41
DES 7 Internet-based education on
pigmented skin lesions
Pre- and postrecognition of
skin lesions
Significant improvement in
correct diagnoses (63%
before and 74% after
P ϭ .002).
Chalabian38
Cohort 120 Intervention group: SCIM on breast
examination; control group: normal
teaching
Breast examination skills Higher score for cohort taught
using SCIM (score 73 v 36;
P ϭ .03)
Campbell37
RCT 54 Intervention group: teaching on breast
examination from standardized
patients; control: normal teaching
Pre- and post-testing of ability
to detect lumps in breast
models
Intervention group higher
sensitivity (71% v 55%;
P ϭ .001), but lower
specificity (48% v 71%;
P ϭ .001)
Pilgrim39
RCT 156 Intervention group: video and lecture
on breast examination plus teaching
from standardized patients; control:
video and lecture only
breast models
detection in intervention
group (P Ͻ .05)
Chart33
RCT 176 Intervention group: standard teaching
on breast examination plus home
study module; control group:
standard teaching
Pre- and postknowledge test;
Scores increased by 2.23 in
intervention group and 0.19 in
control group (P ϭ .001);
positive feedback
Heard40
Int/Con 144 Intervention group: breast examination
teaching by standardized patients;
control: normal teaching
Pre- and postknowledge test
and breast examination skills
Knowledge equivalent;
intervention group had better
clinical skills (84.1% v 69.9%
in OSCE, P Ͻ .001)
Abbreviations: DES, descriptive; NS, not stated; Int/Con, intervention and control arm; RCT, randomized controlled trial; h, hour; Cohort, trial comparing two cohorts
of students; SCIM, structured clinical instruction module; OSCE, objective structured clinical examination.

ofstudieshadcontrolgroups,42
andareviewofpalliativecareteaching
found only descriptive studies.5
Articles are often published in jour-
nals that are not widely available, and many of the interventions are
labor intensive and potentially impractical.
Many of the findings of this review could be applied to the
postgraduate as well as the undergraduate setting, but cancer preven-
tion is a particularly promising area for development in undergradu-
ate education. Cancer prevention education for qualified doctors has
hadvariablesuccess.Afteracourseincervicalandbreastscreening,the
intervention group increased the number of mammograms per-
formed, but reduced the number of cervical screens compared with a
control group. These results were contrary to the author’s expecta-
tions.57
In contrast, the studies described in this review on teaching
cancerpreventiontoundergraduatesaresuccessful.Oncologycourses
might also be particularly relevant to the undergraduate arena, where
they can be used to combat fragmentation of oncology education.58
The authors have some recommendations for capitalizing on
the time and effort put into teaching and learning in oncology.
Teaching knowledge: portfolio learning is at least as successful as a
standard oncology curriculum; computer aided learning is accept-
able. Teaching skills: standardized patients can be used to teach
breast examination; there are manikins available for teaching
breast and testicular examinations; sensitivity for finding lumps in
breast models improves with training; and teaching about cancer
screening and prevention improves cancer prevention skills.
Teaching attitudes: teaching about skin cancer prevention can
change students sun awareness and behavior. Teaching profession-
alism: involvement of patients with cancer benefits the teaching of
communication skills.
There should be more emphasis on performing educational re-
searchinthefieldofoncology.Promisingareasincludecancerpreven-
tion and the standardized use of real patients for teaching.
Table 5. Teaching Communication Skills for Cancer Treatment
Study Design
No. of
Klein46
RCT 249 Intervention group: comm
skills teaching with
patients with cancer;
control group: comm skills
teaching with other
patients
Pre- and postattitude
questionnaire; rating of
student’s interviews with
simulated patients
Positive effect of using
cancer patients on
attitudes and
performance; effect still
detectable at 2 yr
White47
DES 27 (1 ms) Course on breast health
aimed at improving
communication
Pre- and postrating of
interviews with simulated
patients
5% improvement in
scores (P ϭ .039)
Mann48
DES 25 Breast cancer module
involving role play
Student feedback Rating 3.85/5 on a Likert
scale
Keefe49
DES NS Simulations to teach shared
decision making
Formative and summative
assessments (details not
given)
Module is a good teaching
tool (reasons not
stated)
Henry-Tillman60
DES 146 Each student shadowed a
new patient in the breast
clinic
Pre- and postquestionnaire
about knowledge of
empathetic comm
No significant changes in
knowledge of empathy;
variable student
feedback
Hamadeh61
Cohort 70 Short course in truth telling
(ie, paternalism v
autonomy)
Pre- and postquestionnaire on
attitudes to truth telling
Reduction in paternalistic
attitudes
Garg50
DES 359 Course on giving bad news,
including role play
scenarios involving cancer
attitudes to giving bad
news
Increase in the number of
students who had a
plan for giving bad
news (49% to 92%)
Rosenbaum52
DES 341 Small group teaching
involving role play with
standardized patients
Self-reported comfort levels in
giving bad news before,
after, and at 1 yr
Significant increase in
student’s comfort (by
one standard deviation)
Vetto51
Cohort 155 One cohort taught in giving
bad news, one not
Score on OSCE station
involving giving bad news
Score significantly better
in cohort who were
taught (85% v 79%;
P ϭ .05)
Cushing53
DES 231 Course on giving bad news
including role play, video,
simulated patients
Before and after
questionnaire about
knowledge and confidence
in giving bad news
Increase in knowledge
and competence
Colletti55
Int/Con 38 Intervention group: teaching
about giving bad news
(using standardized
patients); control group: no
teaching
Ability to deliver bad news to
a standardized patient;
transferability of skills in
giving bad news
Students in intervention
group performed
significantly better; their
skills were transferable
Farber54
DES 15‫ء‬
Role play using patients with
cancer to teach giving bad
news
attitudes to giving bad
news
Use of real patients
sensitized participants
to the need to use
empathy
Abbreviations: RCT, randomized controlled trial; comm, communication; yr, year; DES, descriptive; ms, medical student; NS, not stated; Cohort, trial comparing two
cohorts of students; OSCE, objective structured clinical examination; Int/Con, intervention and control arm.
‫ء‬
Of the 15 participants all were residents, and seven were in their first year postgraduation.
www.jco.org 1937

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■ ■ ■
Acknowledgment
This research was funded by a grant from Cancer Research United Kingdom. Astrid Mayer and Katherine Woolf assisted with translation
from original French and German articles.
Authors’ Disclosures of Potential Conflicts of Interest
The authors indicated no potential conflicts of interest.
Author Contributions
Conception and design: Judith Gaffan, Jane Dacre, Alison Jones
Administrative support: Judith Gaffan
Provision of study materials or patients: Judith Gaffan
Collection and assembly of data: Judith Gaffan
Data analysis and interpretation: Judith Gaffan, Jane Dacre, Alison Jones
Manuscript writing: Judith Gaffan, Jane Dacre, Alison Jones
Final approval of manuscript: Judith Gaffan, Jane Dacre, Alison Jones
www.jco.org 1939

Editorials
New Horizons in Staging for Non–Small-Cell Lung Cancer
Didier Lardinois (see article on page 1800) ............................................................................................................................................................... 1785
Sentinel Node Micrometastases and Non-Sentinel Nodes in Breast Cancer: How Much
Do We Need to Know?
Harry D. Bear (see article on page 1814) ..................................................................................................................................................................... 1788
Have We Found the Ultimate Risk Factor for Breast Cancer?
Victor G. Vogel and Emanuela Taioli (see article on page 1823) ............................................................................................................. 1791
Cancer in the Elderly Population: The Protection Racket
Derek Raghavan and Theodore Suh (see article on page 1846) ............................................................................................................... 1795
Comments and Controversies
Estrogen Receptor Testing of Breast Cancer in Current Clinical Practice:
What’s the Question?
Stuart J. Schnitt .............................................................................................................................................................................................................................. 1797
Original Reports
LUNG CANCER
Traditional Versus Up-Front [18
F] Fluorodeoxyglucose–Positron Emission Tomography
Staging of Non–Small-Cell Lung Cancer: A Dutch Cooperative Randomized Study
Gerarda J.M. Herder, Henk Kramer, Otto S. Hoekstra, Egbert F. Smit, Jan Pruim, Harm van Tinteren,
Emile F. Comans, Paul Verboom, Carin A. Uyl-de Groot, Alle Welling, Marinus A. Paul, Maarten Boers,
Pieter E. Postmus, Gerrit J. Teule, and Harry J.M. Groen (see editorial on page 1785) ......................................................... 1800
Gefitinib Therapy in Advanced Bronchioloalveolar Carcinoma: Southwest Oncology Group
Study S0126
Howard L. West, Wilbur A. Franklin, Jason McCoy, Paul H. Gumerlock, Ralph Vance, Derick H.M. Lau,
Kari Chansky, John J. Crowley, and David R. Gandara ................................................................................................................................... 1807
JOURNAL OF CLINICAL ONCOLOGY
O f f i c i a l J o u r n a l o f t h e A m e r i c a n S o c i e t y o f C l i n i c a l O n c o l o g y
Vol 24, No 12 C O N T E N T S April 20, 2006
Journal of Clinical Oncology (ISSN 0732-183X) is published 36 times a year, three times monthly, by American Society of Clinical Oncology, 1900 Duke St, Suite 200, Alexandria,
VA 22314. Periodicals postage is paid at Alexandria, VA, and at additional mailing offices. Publication Mail Agreement Number 863289.
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(continued on following page)

BREAST CANCER
Micrometastases in Sentinel Lymph Node in a Multicentric Study: Predictive Factors
of Nonsentinel Lymph Node Involvement—Groupe Des Chirurgiens De La Federation Des
Centres De Lutte Contre Le Cancer
Gilles Houvenaeghel, Claude Nos, Hervé Mignotte, Jean Marc Classe, Sylvie Giard, Philippe Rouanet,
Frédérique Penault Lorca, Jocelyne Jacquemier, and Valérie Jeanne Bardou (see editorial on page 1788) ....... 1814
Endogenous Steroid Hormone Concentrations and Risk of Breast Cancer: Does the
Association Vary by a Woman’s Predicted Breast Cancer Risk?
A. Heather Eliassen, Stacey A. Missmer, Shelley S. Tworoger,
and Susan E. Hankinson (see editorial on page 1791) ..................................................................................................................................... 1823
Docetaxel, Cisplatin, and Trastuzumab As Primary Systemic Therapy for Human
Epidermal Growth Factor Receptor 2–Positive Locally Advanced Breast Cancer
Judith Hurley, Philomena Doliny, Isildinha Reis, Orlando Silva, Carmen Gomez-Fernandez, Pedro Velez,
Giovanni Pauletti, Mark D. Pegram, and Dennis J. Slamon ......................................................................................................................... 1831
Gene Expression Signature Predicting Pathologic Complete Response With Gemcitabine,
Epirubicin, and Docetaxel in Primary Breast Cancer
Olaf Thuerigen, Andreas Schneeweiss, Grischa Toedt, Patrick Warnat, Meinhard Hahn, Heidi Kramer,
Benedikt Brors, Christian Rudlowski, Axel Benner, Florian Schuetz, Bjoern Tews, Roland Eils,
Hans-Peter Sinn, Christof Sohn, and Peter Lichter ............................................................................................................................................. 1839
PHASE I AND CLINICAL PHARMACOLOGY
Prospective Evaluation of the Relationship of Patient Age and Paclitaxel Clinical
Pharmacology: Cancer and Leukemia Group B (CALGB 9762)
Stuart M. Lichtman, Donna Hollis, Antonius A. Miller, Gary L. Rosner, Chris A. Rhoades, Eric P. Lester,
Frederick Millard, John Byrd, Stephen A. Cullinan, D. Marc Rosen, Robert A. Parise, Mark J. Ratain,
and Merrill J. Egorin (see editorial on page 1795) .............................................................................................................................................. 1846
Assessment of Tumor Necrosis Factor Alpha Blockade As an Intervention to Improve
Tolerability of Dose-Intensive Chemotherapy in Cancer Patients
J. Paul Monk, Gary Phillips, Ross Waite, John Kuhn, Larry J. Schaaf, Gregory A. Otterson, Denis Guttridge,
Chris Rhoades, Manisha Shah, Tamara Criswell, Michael A. Caligiuri, and Miguel A. Villalona-Calero .................. 1852
CLINICAL TRIALS
Factors Associated With Participation in Breast Cancer Treatment Clinical Trials
Nancy E. Avis, Kevin W. Smith, Carol L. Link, Gabriel N. Hortobagyi, and Edgardo Rivera .............................................. 1860
GENITOURINARY CANCER
Immediate or Deferred Androgen Deprivation for Patients With Prostate Cancer Not
Suitable for Local Treatment With Curative Intent: European Organisation for Research
and Treatment of Cancer (EORTC) Trial 30891
Urs E. Studer, Peter Whelan, Walter Albrecht, Jacques Casselman, Theo de Reijke, Dieter Hauri,
Wolfgang Loidl, Santiago Isorna, Subramanian K. Sundaram, Muriel Debois, and Laurence Collette ..................... 1868
SURGICAL ONCOLOGY
Dermoscopy Improves Accuracy of Primary Care Physicians to Triage Lesions
Suggestive of Skin Cancer
Giuseppe Argenziano, Susana Puig, Iris Zalaudek, Francesco Sera, Rosamaria Corona, Merce` Alsina,
Filomena Barbato, Cristina Carrera, Gerardo Ferrara, Antonio Guilabert, Daniela Massi,
Juan A. Moreno-Romero, Carlos Mun˜ oz-Santos, Gianluca Petrillo, Sonia Segura, H. Peter Soyer,
Renato Zanchini, and Josep Malvehy ........................................................................................................................................................................... 1877

GASTROINTESTINAL CANCER
Pharmacogenetic Profiling and Clinical Outcome of Patients With Advanced Gastric
Cancer Treated With Palliative Chemotherapy
Annamaria Ruzzo, Francesco Graziano, Kazuyuki Kawakami, Go Watanabe, Daniele Santini,
Vincenzo Catalano, Renato Bisonni, Emanuele Canestrari, Rita Ficarelli, Ettore Tito Menichetti, Davide Mari,
Enrica Testa, Rosarita Silva, Bruno Vincenzi, Paolo Giordani, Stefano Cascinu, Lucio Giustini,
Giuseppe Tonini, and Mauro Magnani ......................................................................................................................................................................... 1883
Phase II Study of Capecitabine, Oxaliplatin, and Erlotinib in Previously Treated Patients
With Metastastic Colorectal Cancer
Jeffrey A. Meyerhardt, Andrew X. Zhu, Peter C. Enzinger, David P. Ryan, Jeffrey W. Clark,
Matthew H. Kulke, Craig C. Earle, Michele Vincitore, Ann Michelini, Susan Sheehan, and Charles S. Fuchs ..... 1892
Phase II Study of Gemcitabine and Oxaliplatin in Combination With Bevacizumab in
Patients With Advanced Hepatocellular Carcinoma
Andrew X. Zhu, Lawrence S. Blaszkowsky, David P. Ryan, Jeffrey W. Clark, Alona Muzikansky,
Kerry Horgan, Susan Sheehan, Kelly E. Hale, Peter C. Enzinger, Pankaj Bhargava, and Keith Stuart ....................... 1898
SUPPORTIVE CARE AND QUALITY OF LIFE
Sensorineural Hearing Loss After Radiotherapy and Chemoradiotherapy: A Single,
Blinded, Randomized Study
Wong Kein Low, Song Tar Toh, Joseph Wee, Stephanie M.C. Fook-Chong, and De Yun Wang ................................... 1904
TUMOR BIOLOGY
Chemokine Receptor CCR6 Expression Level and Liver Metastases in Colorectal Cancer
Pirus Ghadjar, Sarah Ellen Coupland, Il-Kang Na, Michel Noutsias, Anne Letsch, Andrea Stroux,
Sandra Bauer, Heinz J. Buhr, Eckhard Thiel, Carmen Scheibenbogen, and Ulrich Keilholz .............................................. 1910
PEDIATRIC ONCOLOGY
Phase II Study of Clofarabine in Pediatric Patients With Refractory or Relapsed Acute
Lymphoblastic Leukemia
Sima Jeha, Paul S. Gaynon, Bassem I. Razzouk, Janet Franklin, Richard Kadota, Violet Shen,
Lori Luchtman-Jones, Michael Rytting, Lisa R. Bomgaars, Susan Rheingold, Kim Ritchey, Edythe Albano,
Robert J. Arceci, Stewart Goldman, Timothy Griffin, Arnold Altman, Bruce Gordon, Laurel Steinherz,
Steven Weitman, and Peter Steinherz ........................................................................................................................................................................... 1917
Genomics Identifies Medulloblastoma Subgroups That Are Enriched for Specific
Genetic Alterations
Margaret C. Thompson, Christine Fuller, Twala L. Hogg, James Dalton, David Finkelstein, Ching C. Lau,
Murali Chintagumpala, Adekunle Adesina, David M. Ashley, Stewart J. Kellie, Michael D. Taylor,
Tom Curran, Amar Gajjar, and Richard J. Gilbertson ....................................................................................................................................... 1924
Review Article
Educating Undergraduate Medical Students About Oncology: A Literature Review
Judith Gaffan, Jane Dacre, and Alison Jones ......................................................................................................................................................... 1932
Special Article
Recommendations From an International Expert Panel on the Use of Neoadjuvant
(Primary) Systemic Treatment of Operable Breast Cancer: An Update
Manfred Kaufmann, Gabriel N. Hortobagyi, Aron Goldhirsch, Suzy Scholl, Andreas Makris,
Pinuccia Valagussa, Jens-Uwe Blohmer, Wolfgang Eiermann, Raimund Jackesz, Walter Jonat,
Annette Lebeau, Sibylle Loibl, William Miller, Sigfried Seeber, Vladimir Semiglazov, Roy Smith,
Rainer Souchon, Vered Stearns, Michael Untch, and Gunter von Minckwitz ................................................................................ 1940
Diagnosis in Oncology
Large B-Cell Lymphoma Masquerading As Acute Leukemia
Joanna Steere, Alexander Perl, Ewa Tomczak, and Adam Bagg ............................................................................................................. 1950

Acute Lung Injury Associated With Vinorelbine
Tawee Tanvetyanon, Edward R. Garrity, and Kathy S. Albain ................................................................................................................... 1952
Laryngeal Obstruction and Hoarseness Associated With Rosai-Dorfman Disease
Furha Cossor, Al-Hareth M. Al-Khater, and Donald C. Doll .......................................................................................................................... 1953
Aromatase Inhibitor Withdrawal Response in Metastatic Breast Cancer
Tessa Cigler and Paul E. Goss ............................................................................................................................................................................................. 1955
Correspondence
New Issues on Cetuximab Mechanism of Action in Epidermal Growth Factor Receptor–
Negative Colorectal Cancer: The Role of Vascular Endothelial Growth Factor
Bruno Vincenzi, Daniele Santini, and Giuseppe Tonini ................................................................................................................................... 1957
In Reply
Ki Young Chung and Leonard B. Saltz .......................................................................................................................................................................... 1957
Childhood Nonrhabdomyosarcoma Soft Tissue Sarcomas Are Not Adult-Type Tumors
Sheri L. Spunt and Alberto S. Pappo ............................................................................................................................................................................. 1958
In Reply
Laurence H. Baker ......................................................................................................................................................................................................................... 1959
Is It Time to Abandon Microsatellite Instability As a Pre-Screen for Selecting Families
for Mutation Testing for Mismatch Repair Genes?
Gareth D. Evans, Fiona Lalloo, Tony Mak, Doug Speake, and James Hill ........................................................................................ 1960
In Reply
Melissa C. Southey, Mark A. Jenkins, John L. Hopper, Finlay A. Macrae, and Graham G. Giles .................................. 1962
Overestimating the Inﬂuence of the 1999 WHO Classiﬁcation of Lung Tumors on Survival
in Bronchioloalveloar Carcinoma
Junji Tsurutani, Marc S. Ballas, and Phillip A. Dennis ..................................................................................................................................... 1963
In Reply
Jason A. Zell, Sai-Hong Ignatius Ou, Argyrios Ziogas, and Hoda Anton-Culver ......................................................................... 1963
Are We Cautious Enough When We Interpret Results of Randomized But
Underpowered Comparisons?
Marianne Paesmans and Harry Bleiberg ..................................................................................................................................................................... 1964
In Utero Exposure to Chemotherapy: Effect on Cardiac and Neurologic Outcome
Kristel Van Calsteren, Patrick Berteloot, Myriam Hanssens, Ignace Vergote, Frederic Amant,
Javier Ganame, Piet Claus, Luc Mertens, Lieven Lagae, Michel Delforge, Robert Paridaens, Lucien Noens,
Yves Humblet, Bruno Vandermeersch, and Xavier De Muylder .............................................................................................................. e16
Errata .................................................................................................................................................................................................................................................... 1966
Also in This Issue
Announcements
Information for Contributors
Current Abstracts
Calendar of Oncology Events
Online supplementary information available at www.jco.org
Article was published online ahead of print at www.jco.org
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